{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:01:18Z","timestamp":1760122878916,"version":"3.41.2"},"reference-count":63,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2019,9,4]],"date-time":"2019-09-04T00:00:00Z","timestamp":1567555200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"DOI":"10.3389\/fimmu.2019.02006","type":"journal-article","created":{"date-parts":[[2019,9,4]],"date-time":"2019-09-04T12:23:51Z","timestamp":1567599831000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":7,"title":["Prime-Boost Vaccination With a Novel Hemagglutinin Protein Produced in Bacteria Induces Neutralizing Antibody Responses Against H5-Subtype Influenza Viruses in Commercial Chickens"],"prefix":"10.3389","volume":"10","author":[{"given":"Violetta","family":"S\u0105czy\u0144ska","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Agnieszka","family":"Romanik-Chru\u015bcielewska","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Katarzyna","family":"Florys","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Violetta","family":"Cecuda-Adamczewska","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Natalia","family":"\u0141ukasiewicz","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Iwona","family":"Soko\u0142owska","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ma\u0142gorzata","family":"K\u0119sik-Brodacka","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gra\u017cyna","family":"P\u0142ucienniczak","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2019,9,4]]},"reference":[{"unstructured":"WorldOrganization for Animal Health OIE Situation Report for Highly Pathogenic Avian Influenza. OIE.2018","key":"B1"},{"key":"B2","doi-asserted-by":"publisher","first-page":"842","DOI":"10.3201\/eid2105.141927","article-title":"Rapid emergence of highly pathogenic avian influenza subtypes from a subtype H5N1 hemagglutinin variant","volume":"21","author":"de Vries","year":"2015","journal-title":"Emerg Infect Dis."},{"unstructured":"Cumulative Number of Confirmed Human Cases for Avian Influenza A(H5N1) Reported to WHO, 2003\u20132018.2018","key":"B3"},{"key":"B4","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1136\/vr.g6101","article-title":"FAO warns of new strain of avian influenza virus","volume":"175","year":"2014","journal-title":"Vet Rec"},{"key":"B5","doi-asserted-by":"publisher","first-page":"886","DOI":"10.3201\/eid2105.142020","article-title":"Novel Eurasian highly pathogenic avian influenza A H5 viruses in wild birds, Washington, USA, 2014","volume":"21","author":"Ip","year":"2015","journal-title":"Emerg Infect Dis"},{"key":"B6","doi-asserted-by":"publisher","first-page":"741","DOI":"10.1126\/science.348.6236.741","article-title":"Avian influenza. Enigmatic bird flu strain races across the U.S. Midwest","volume":"348","author":"Hvistendahl","year":"2015","journal-title":"Science"},{"key":"B7","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/j.virusres.2013.03.004","article-title":"Vaccination of gallinaceous poultry for H5N1 highly pathogenic avian influenza: current questions and new technology","volume":"178","author":"Spackman","year":"2013","journal-title":"Virus Res"},{"key":"B8","doi-asserted-by":"publisher","first-page":"408","DOI":"10.1016\/j.tvjl.2014.09.017","article-title":"Practical aspects of vaccination of poultry against avian influenza virus","volume":"202","author":"Spackman","year":"2014","journal-title":"Vet J"},{"key":"B9","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1159\/000325276","article-title":"Current status and future needs in diagnostics and vaccines for high pathogenicity avian influenza","volume":"135","author":"Swayne","year":"2013","journal-title":"Dev Biol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"737","DOI":"10.1146\/annurev.iy.08.040190.003513","article-title":"Structural basis of immune recognition of influenza virus hemagglutinin","volume":"8","author":"Wilson","year":"1990","journal-title":"Annu Rev Immunol"},{"key":"B11","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1007\/s11259-018-9717-1","article-title":"Effectiveness of different avian influenza (H5) vaccination regimens in layer chickens on the humoral immune response and interferon-alpha signalling immune marker","volume":"42","author":"Hamad","year":"2018","journal-title":"Vet Res Commun"},{"key":"B12","doi-asserted-by":"publisher","first-page":"5760","DOI":"10.1016\/j.vaccine.2013.08.064","article-title":"Evaluation of safety and immunogenicity of recombinant influenza hemagglutinin (H5\/Indonesia\/05\/2005) formulated with and without a stable oil-in-water emulsion containing glucopyranosyl-lipid A (SE+GLA) adjuvant","volume":"31","author":"Treanor","year":"2013","journal-title":"Vaccine"},{"key":"B13","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1016\/j.biologicals.2005.08.003","article-title":"Overview of avian influenza DIVA test strategies","volume":"33","author":"Suarez","year":"2005","journal-title":"Biologicals"},{"key":"B14","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/S0092-8674(00)81771-7","article-title":"Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation","volume":"95","author":"Chen","year":"1998","journal-title":"Cell"},{"key":"B15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1006\/viro.1999.9716","article-title":"Role of hemagglutinin cleavage for the pathogenicity of influenza virus","volume":"258","author":"Steinhauer","year":"1999","journal-title":"Virology"},{"key":"B16","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1083\/jcb.103.4.1179","article-title":"Assembly of influenza hemagglutinin trimers and its role in intracellular transport","volume":"103","author":"Copeland","year":"1986","journal-title":"J Cell Biol"},{"key":"B17","doi-asserted-by":"crossref","first-page":"3048","DOI":"10.1128\/JVI.67.6.3048-3060.1993","article-title":"Role of conserved glycosylation sites in maturation and transport of influenza A virus hemagglutinin","volume":"67","author":"Roberts","year":"1993","journal-title":"J Virol"},{"key":"B18","doi-asserted-by":"publisher","first-page":"6200","DOI":"10.1128\/JVI.00187-08","article-title":"Comparative efficacy of neutralizing antibodies elicited by recombinant hemagglutinin proteins from avian H5N1 influenza virus","volume":"82","author":"Wei","year":"2008","journal-title":"J Virol"},{"key":"B19","doi-asserted-by":"publisher","first-page":"e10645","DOI":"10.1371\/journal.pone.0010645","article-title":"A single immunization with soluble recombinant trimeric hemagglutinin protects chickens against highly pathogenic avian influenza virus H5N1","volume":"5","author":"Cornelissen","year":"2010","journal-title":"PLoS ONE"},{"key":"B20","doi-asserted-by":"publisher","first-page":"10366","DOI":"10.1128\/JVI.01035-10","article-title":"Recombinant soluble, multimeric HA and NA exhibit distinctive types of protection against pandemic swine-origin 2009 A(H1N1) influenza virus infection in ferrets","volume":"84","author":"Bosch","year":"2010","journal-title":"J Virol"},{"key":"B21","doi-asserted-by":"publisher","first-page":"11735","DOI":"10.1128\/JVI.01084-12","article-title":"Glycan-dependent immunogenicity of recombinant soluble trimeric hemagglutinin","volume":"86","author":"de Vries","year":"2012","journal-title":"J Virol"},{"key":"B22","doi-asserted-by":"crossref","first-page":"2265","DOI":"10.1016\/S0264-410X(98)00494-0","article-title":"Baculovirus-derived hemagglutinin vaccines protect against lethal influenza infections by avian H5 and H7 subtypes","volume":"17","author":"Crawford","year":"1999","journal-title":"Vaccine"},{"key":"B23","doi-asserted-by":"publisher","first-page":"1147","DOI":"10.1292\/jvms.70.1147","article-title":"Baculovirus-derived hemagglutinin vaccine protects chickens from lethal homologous virus H5N1 challenge","volume":"70","author":"Lin","year":"2008","journal-title":"J Vet Med Sci"},{"key":"B24","doi-asserted-by":"publisher","first-page":"e12466","DOI":"10.1371\/journal.pone.0012466","article-title":"Enhanced immunogenicity of stabilized trimeric soluble influenza hemagglutinin","volume":"5","author":"Weldon","year":"2010","journal-title":"PLoS ONE"},{"key":"B25","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1016\/j.antiviral.2016.08.001","article-title":"An avian influenza H5N1 virus vaccine candidate based on the extracellular domain produced in yeast system as subviral particles protects chickens from lethal challenge","volume":"133","author":"Pietrzak","year":"2016","journal-title":"Antiviral Res"},{"key":"B26","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/j.virusres.2017.01.025","article-title":"A prime\/boost vaccination with HA DNA and Pichia-produced HA protein elicits a strong humoral response in chickens against H5N1","volume":"232","author":"Stachyra","year":"2017","journal-title":"Virus Res"},{"key":"B27","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1038\/289366a0","article-title":"Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution","volume":"289","author":"Wilson","year":"1981","journal-title":"Nature"},{"key":"B28","doi-asserted-by":"publisher","first-page":"561","DOI":"10.18388\/abp.2014_1878","article-title":"Influenza virus hemagglutinin as a vaccine antigen produced in bacteria","volume":"61","author":"S\u0105czy\u0144ska","year":"2014","journal-title":"Acta Biochim Pol"},{"key":"B29","doi-asserted-by":"publisher","first-page":"18137","DOI":"10.1073\/pnas.0909696106","article-title":"Glycans on influenza hemagglutinin affect receptor binding and immune response","volume":"106","author":"Wang","year":"2009","journal-title":"Proc Natl Acad Sci USA"},{"key":"B30","doi-asserted-by":"publisher","first-page":"e2257","DOI":"10.1371\/journal.pone.0002257","article-title":"Efficacious recombinant influenza vaccines produced by high yield bacterial expression: a solution to global pandemic and seasonal needs","volume":"3","author":"Song","year":"2008","journal-title":"PLoS ONE"},{"key":"B31","doi-asserted-by":"publisher","first-page":"997","DOI":"10.1007\/s13238-011-1134-y","article-title":"Structural vaccinology: structure-based design of influenza A virus hemagglutinin subtype-specific subunit vaccines","volume":"2","author":"Xuan","year":"2011","journal-title":"Protein Cell"},{"key":"B32","doi-asserted-by":"publisher","first-page":"e78947","DOI":"10.1371\/journal.pone.0078947","article-title":"Bacterially produced recombinant influenza vaccines based on virus-like particles","volume":"8","author":"Jegerlehner","year":"2013","journal-title":"PLoS ONE"},{"key":"B33","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.bbrc.2009.03.106","article-title":"Immunological study of HA1 domain of hemagglutinin of influenza H5N1 virus","volume":"383","author":"Chiu","year":"2009","journal-title":"Biochem Biophys Res Commun"},{"key":"B34","first-page":"171","article-title":"The role of the antibody response in influenza virus infection","volume":"260","author":"Gerhard","year":"2001","journal-title":"Curr Top Microbiol Immunol"},{"key":"B35","doi-asserted-by":"publisher","first-page":"34","DOI":"10.4161\/hv.8.1.18214","article-title":"Correlates of vaccine protection from influenza and its complications","volume":"8","author":"McCullers","year":"2012","journal-title":"Hum Vaccin Immunother"},{"key":"B36","doi-asserted-by":"publisher","first-page":"6833","DOI":"10.1016\/j.vaccine.2012.09.013","article-title":"Flagellin-HA vaccines protect ferrets and mice against H5N1 highly pathogenic avian influenza virus (HPAIV) infections","volume":"30","author":"Liu","year":"2012","journal-title":"Vaccine"},{"key":"B37","doi-asserted-by":"publisher","first-page":"5393","DOI":"10.1016\/j.vaccine.2008.07.084","article-title":"H5N1 VLP vaccine induced protection in ferrets against lethal challenge with highly pathogenic H5N1 influenza viruses","volume":"26","author":"Mahmood","year":"2008","journal-title":"Vaccine"},{"key":"B38","doi-asserted-by":"publisher","first-page":"4299","DOI":"10.1016\/j.vaccine.2008.06.012","article-title":"FDA\/NIH\/WHO public workshop on immune correlates of protection against influenza A viruses in support of pandemic vaccine development, Bethesda, Maryland, US, December 10-11, 2007","volume":"26","author":"Eichelberger","year":"2008","journal-title":"Vaccine"},{"key":"B39","doi-asserted-by":"publisher","first-page":"405","DOI":"10.4161\/hv.22908","article-title":"Correlates of protection to influenza virus, where do we go from here?","volume":"9","author":"Cox","year":"2013","journal-title":"Hum Vaccin Immunother"},{"key":"B40","doi-asserted-by":"publisher","first-page":"1369","DOI":"10.1586\/14760584.2013.850036","article-title":"The emergence of H7N9 viruses: a chance to redefine correlates of protection for influenza virus vaccines","volume":"12","author":"Krammer","year":"2013","journal-title":"Expert Rev Vaccines"},{"key":"B41","doi-asserted-by":"publisher","first-page":"e0172008","DOI":"10.1371\/journal.pone.0172008","article-title":"A novel hemagglutinin protein produced in bacteria protects chickens against H5N1 highly pathogenic avian influenza viruses by inducing H5 subtype-specific neutralizing antibodies","volume":"12","author":"S\u0105czy\u0144ska","year":"2017","journal-title":"PLoS ONE"},{"key":"B42","doi-asserted-by":"publisher","first-page":"E2","DOI":"10.3390\/v10010002","article-title":"Broadening the H5N3 vaccine immunogenicity against H5N1 virus by modification of neutralizing epitopes","volume":"10","author":"Rajesh Kumar","year":"2017","journal-title":"Viruses"},{"key":"B43","doi-asserted-by":"publisher","first-page":"496","DOI":"10.1126\/science.aan0516","article-title":"Potent peptidic fusion inhibitors of influenza virus","volume":"358","author":"Kadam","year":"2017","journal-title":"Science"},{"key":"B44","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1186\/1475-2859-11-109","article-title":"A novel system for stable, high-level expression from the T7 promoter","volume":"11","author":"Kesik-Brodacka","year":"2012","journal-title":"Microb Cell Fact"},{"key":"B45","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1186\/s12985-017-0886-2","article-title":"Production of highly and broad-range specific monoclonal antibodies against hemagglutinin of H5-subtype avian influenza viruses and their differentiation by mass spectrometry","volume":"15","author":"S\u0105czy\u0144ska","year":"2018","journal-title":"Virol J"},{"unstructured":"Manual of Diagnostic Tests and Vaccines for Terrestrial Animals.2012","key":"B46"},{"unstructured":"2017","key":"B47"},{"key":"B48","doi-asserted-by":"publisher","first-page":"728","DOI":"10.3382\/ps\/pev015","article-title":"Consequences of different growth rates in broiler breeder and layer hens on embryogenesis, metabolism and metabolic rate: a review","volume":"94","author":"Buza\u0142a","year":"2015","journal-title":"Poult Sci"},{"key":"B49","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/S0165-2427(02)00169-1","article-title":"Immunological differences between layer- and broiler-type chickens","volume":"89","author":"Koenen","year":"2002","journal-title":"Vet Immunol Immunopathol"},{"key":"B50","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.coi.2013.12.007","article-title":"Immunomodulatory properties of the vaccine adjuvant alum","volume":"28","author":"Oleszycka","year":"2014","journal-title":"Curr Opin Immunol"},{"key":"B51","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/S0065-3519(99)80036-6","article-title":"Introduction to poultry vaccines and immunity","volume":"41","author":"Sharma","year":"1999","journal-title":"Adv Vet Med"},{"key":"B52","doi-asserted-by":"publisher","first-page":"1294","DOI":"10.3390\/v6031294","article-title":"Playing hide and seek: how glycosylation of the influenza virus hemagglutinin can modulate the immune response to infection","volume":"6","author":"Tate","year":"2014","journal-title":"Viruses"},{"key":"B53","doi-asserted-by":"publisher","first-page":"7436","DOI":"10.1074\/jbc.M114.620534","article-title":"Immunosilencing a highly immunogenic protein trimerization domain","volume":"290","author":"Sliepen","year":"2015","journal-title":"J Biol Chem"},{"key":"B54","doi-asserted-by":"publisher","first-page":"1246","DOI":"10.1128\/JVI.02107-10","article-title":"Bacterial HA1 vaccine against pandemic H5N1 influenza virus: evidence of oligomerization, hemagglutination, and cross-protective immunity in ferrets","volume":"85","author":"Khurana","year":"2011","journal-title":"J Virol"},{"key":"B55","doi-asserted-by":"publisher","first-page":"12283","DOI":"10.1128\/JVI.01596-12","article-title":"Oligomeric recombinant H5 HA1 vaccine produced in bacteria protects ferrets from homologous and heterologous wild-type H5N1 influenza challenge and controls viral loads better than subunit H5N1 vaccine by eliciting high-affinity antibodies","volume":"86","author":"Verma","year":"2012","journal-title":"J Virol"},{"key":"B56","doi-asserted-by":"publisher","first-page":"59","DOI":"10.4161\/hv.8.1.18011","article-title":"Adjuvanted influenza vaccines","volume":"8","author":"Principi","year":"2012","journal-title":"Hum Vaccin Immunother"},{"key":"B57","doi-asserted-by":"publisher","first-page":"1608","DOI":"10.3382\/ps.2009-00092","article-title":"Preparation and immune activity analysis of H5N1 subtype avian influenza virus recombinant protein-based vaccine","volume":"88","author":"Xie","year":"2009","journal-title":"Poult Sci"},{"key":"B58","doi-asserted-by":"crossref","first-page":"2666","DOI":"10.1016\/S0264-410X(00)00498-9","article-title":"Adjuvants designed for veterinary and human vaccines","volume":"19","author":"Aucouturier","year":"2001","journal-title":"Vaccine"},{"key":"B59","doi-asserted-by":"publisher","first-page":"3401","DOI":"10.1016\/j.vaccine.2017.05.010","article-title":"Immunologic evaluation of 10 different adjuvants for use in vaccines for chickens against highly pathogenic avian influenza virus","volume":"35","author":"Lone","year":"2017","journal-title":"Vaccine"},{"key":"B60","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1080\/03079451003604639","article-title":"Efficacy of infectious bronchitis virus vaccinations in the field: association between the alpha-IBV IgM response, protection and vaccine application parameters","volume":"39","author":"De Wit","year":"2010","journal-title":"Avian Pathol"},{"key":"B61","doi-asserted-by":"publisher","first-page":"E135","DOI":"10.3390\/v11020135","article-title":"Effect of pullet vaccination on development and longevity of immunity","volume":"11","author":"Aston","year":"2019","journal-title":"Viruses"},{"unstructured":"2019","key":"B62"},{"key":"B63","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1016\/B978-012370634-8.50023-8","article-title":"Practical aspects of poultry vaccination","volume-title":"Avian Immunology.","author":"Schijns","year":"2008"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2019.02006\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,1,18]],"date-time":"2021-01-18T04:26:16Z","timestamp":1610943976000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2019.02006\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,9,4]]},"references-count":63,"alternative-id":["10.3389\/fimmu.2019.02006"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2019.02006","relation":{},"ISSN":["1664-3224"],"issn-type":[{"type":"electronic","value":"1664-3224"}],"subject":[],"published":{"date-parts":[[2019,9,4]]},"article-number":"2006"}}